The tubulin and histone genes of <i>Physarum polycephalum</i>: Models for cell cycle‐regulated gene expression

Laffler, Thomas G.; Carrino, John J.

doi:10.1002/bies.950050205

Cited by 10 publications

(4 citation statements)

References 19 publications

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“…Tubulin genes of Physarum polycephalum are periodically expressed during the naturally synchronous mitotic cycle of the plasmodial phase [1][2][3]. Their expression is also governed by a developmental switch during the transition from the myxamoebal to the plasmodial phase of the life-cycle [4,51. We have cloned and sequenced the Nc~-tubulin gene which is expressed in plasmodia but not in myxamoebae.…”

Section: Introductionmentioning

confidence: 99%

Identification of EcoRV fragments spanning the Nα‐tubulin gene of Physarum

1988

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The N~t-tubulin gene of Physarum polycephalum has an EcoRV site at codons 252/253. EcoRV digestion of Physarum DNA generated two EcoRV fragments per gene copy comprising both coding and flanking sequences. Hybridisation probes which included coding sequences upstream from the central EcoRV site cross-hybridised with another ct-tubulin gene. Probes derived from either 5'-or 3'-flanking regions were gene-specific. These probes identified two EcoRV fragments in the haploid strain CLdAXE viz 5.4 kb (5'-fragment) and 6.2 kb (3'-fragment). The same two fragments were identified in EcoRV digests of DNA of the diploid strain M3CVIII, and a second form of the gene was also identified comprising two fragments viz 5.0 kb (5'-end) and 5.5 kb (T-end). Both forms gave rise to an identical 4.65 kb HindlII fragment as judged by restriction mapping.

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Section: Introductionmentioning

confidence: 99%

Identification of EcoRV fragments spanning the Nα‐tubulin gene of Physarum

1988

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“…This provides an excellent system in which to study cell cycle periodicities. The Physarum cell cycle has been the subject of two recent reviews (8,10).…”

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confidence: 99%

“…We have recently described the pattern of a-tubulin and histone H4 mRNA accumulation and gene transcription during the Physarum cell cycle (2,8). Transcription of both genes increases dramatically in mid-G2 phase in preparation for mitosis and entry into the S phase.…”

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Distinct replication-independent and -dependent phases of histone gene expression during the Physarum cell cycle.

Carrino¹,

Kueng²,

Braun³

et al. 1987

Mol. Cell. Biol.

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During the S phase of the cell cycle, histone gene expression and DNA replication are tightly coupled. In mitotically synchronous plasmodia of the myxomycete Physarum polycephalum, which has no G1 phase, histone mRNA synthesis begins in mid-G2 phase. Although histone gene transcription is activated in the absence of significant DNA synthesis, our data demonstrate that histone gene expression became tightly coupled to DNA replication once the S phase began. There was a transition from the replication-independent phase to the replication-dependent phase of histone gene expression. During the first phase, histone mRNA synthesis appears to be under direct cell cycle control; it was not coupled to DNA replication. This allowed a pool of histone mRNA to accumulate in late G2 phase, in anticipation of future demand. The second phase began at the end of mitosis, when the S phase began, and expression became homeostatically coupled to DNA replication. This homeostatic control required continuing protein synthesis, since cycloheximide uncoupled transcription from DNA synthesis. Nuclear run-on assays suggest that in P. polycephalum this coupling occurs at the level of transcription. While histone gene transcription appears to be directly switched on in mid-G2 phase and off at the end of the S phase by cell cycle regulators, only during the S phase was the level of transcription balanced with the rate of DNA synthesis.

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“…In a recent review, we proposed three major transition points involved in regulating periodic histone gene expression within the P. polycephalum cell cycle (4). The first occurs in the early G2 phase, when plasmodia begin transcribing the histone genes.…”

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Cell-cycle-regulated translation of histone mRNA in Physarum plasmodia

Laffler¹,

Carrino²

1987

J Bacteriol

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In Physarum polycephalum, histone mRNA begins to accumulate 3 h before the S phase. We show that histone synthesis was limited to the S phase and that the mRNA that accumulated in the G2-phase cytoplasm could be translated in vitro. Thus, recruitment of stored mature histone mRNA did not occur until the S phase began.Histone gene expression has proven to be cell cycle regulated in virtually every eucaryote studied. Namely, synthesis of the core histones is limited to the S phase in organisms ranging from yeasts to humans. Generally, an increase in the level of histone mRNA parallels the peak of histone protein synthesis, although many species store pools of inactive maternal messenger in the oocyte nucleus for recruitment later during embryogenesis (for a review, see reference 7). Here, we report a unique exception to this rule.These experiments with mitotically synchronous plasmodia of the primitive myxomycete Physarum polycephalum show that histone mRNA is regularly stored during the G2 phase of its mitotic cycle. Since the P. polycephalum cell cycle has no Gi phase, its S phase begins at the end of mitosis. We have reported that both transcription of the histone genes and accumulation of histone mRNA begin with an event in early to mid-G2 phase, about 3 h before the S phase begins (1). The maximum accumulation of histone mRNA occurs at the end of the G2 phase, in the absence of significant DNA synthesis. While histone gene expression is clearly cell cycle regulated in P. polycephalum, mRNA accumulation is not dependent on DNA replication (1). Transcription of these genes is directly regulated by a cell cycle control mechanism rather than occurring as an indirect response to increased demand for the histone proteins during the S phase (1).This note addresses the storage and activity of the G2-phase histone mRNA. The G2-phase accumulation of histone mRNA serves a useful purpose; it provides a dowry of mRNA to meet the maximum demand for new histone proteins that occurs at the beginning of the S phase. While preliminary studies of histone protein synthesis in P. polycephalum show that histone synthesis peaks in the S phase, the investigators failed to study histone synthesis in the last hour of the G2 phase (9). This left open the possibility that a dowry of histone proteins might accumulate before the S phase begins. The data presented below show that this did not occur; histone synthesis was limited to the S phase. Wilhelm et al. (10) reported an apparent shortening of histone H4 mRNA at the beginning of the S phase. Since this might reflect a change in the primary structure of the mRNA needed for its efficient translation, we compared the translatability of G2-phase and S-phase mRNAs in wheat germ extracts. Our data indicate that the efficiencies of translation were comparable. In addition, we show that the * Corresponding author.histone mRNA was stored in the G2-phase cytoplasm rather than in the nucleus. Therefore, we infer that during the G2 phase, mature histone mRNA is stored in the cytoplasm as a tr...

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The tubulin and histone genes of Physarum polycephalum: Models for cell cycle‐regulated gene expression

Cited by 10 publications

References 19 publications

Identification of EcoRV fragments spanning the Nα‐tubulin gene of Physarum

Identification of EcoRV fragments spanning the Nα‐tubulin gene of Physarum

Distinct replication-independent and -dependent phases of histone gene expression during the Physarum cell cycle.

Cell-cycle-regulated translation of histone mRNA in Physarum plasmodia

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